Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T07:05:21.821Z Has data issue: false hasContentIssue false
  • English
  • Français

Glucose in a maturation medium with reduced NaCl improves oocyte maturation and embryonic development after somatic cell nuclear transfer and in vitro fertilization in pigs

Published online by Cambridge University Press:  03 March 2021

Yongjin Lee ,
Hanna Lee ,
Joohyeong Lee ,
Seung Tae Lee ,
Geun-Shik Lee  and
Eunsong Lee Open the ORCID record for Eunsong Lee [Opens in a new window]
Yongjin Lee
Affiliation:
College of Veterinary Medicine, Kangwon National University, Chuncheon24341, Korea
Hanna Lee
Affiliation:
College of Veterinary Medicine, Kangwon National University, Chuncheon24341, Korea
Joohyeong Lee
Affiliation:
Institute of Veterinary Science, Kangwon National University, Chuncheon24341, Korea
Seung Tae Lee
Affiliation:
Division of Applied Animal Science, Kangwon National University, Chuncheon24341, Korea
Geun-Shik Lee
Affiliation:
College of Veterinary Medicine, Kangwon National University, Chuncheon24341, Korea
Eunsong Lee*
Affiliation:
College of Veterinary Medicine, Kangwon National University, Chuncheon24341, Korea Institute of Veterinary Science, Kangwon National University, Chuncheon24341, Korea
*
Author for correspondence: Eunsong Lee. College of Veterinary Medicine, Kangwon National University, Chuncheon24341, Korea. Tel: +82 33 250 8670. Fax: +82 33 259 5625. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study was conducted to examine whether glucose in maturation medium containing reduced NaCl could improve oocyte maturation and embryonic development in pigs. The base medium was bovine serum albumin-free porcine zygote medium (PZM)-3 containing 10% (v/v) pig follicular fluid (FPZM) or 0.1% (w/v) polyvinyl alcohol (PPZM). Using each medium, the effects of NaCl concentrations (108 and 61.6 mM) and 5.56 mM glucose supplementation (designated as PZM108N, PZM108G, PZM61N, and PZM61G, respectively) were examined using a 2 × 2 factorial arrangement. When oocytes were matured in FPZM, glucose supplementation improved nuclear maturation compared with no supplementation, regardless of the NaCl concentrations. FPZM61G showed a higher blastocyst formation compared with FPZM108N and FPZM108G after parthenogenesis (PA). Blastocyst formations of somatic cell nuclear transfer (SCNT) embryos derived from FPZM61N and FPZM61G were higher compared with those of oocytes from FPZM108N. When oocytes were matured in PPZM, glucose added to PPZM108 and PPZM61 increased nuclear maturation compared with no supplementation. However, glucose added to PPZM108 did not alter embryonic development after PA. Additionally, oocytes matured in PPZM61G showed a higher blastocyst formation compared with those from PPZM61N. In SCNT, blastocyst formation was not influenced by glucose supplementation of PPZM108, but was increased by maturation in glucose-supplemented PPZM61. In embryonic development of in vitro fertilization (IVF), oocytes matured in medium with reduced NaCl and glucose showed significantly higher blastocyst formation compared with those matured in PPZM108G. Our results demonstrated that glucose in maturation medium containing 61.6 mM NaCl increased oocyte maturation and embryonic development after PA, SCNT, and IVF.

Keywords

Defined mediumGlucoseNuclear transferOocyte maturationReduced NaCl
Type
Research Article
Information
Zygote , Volume 29 , Issue 4 , August 2021 , pp. 293 - 300
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These two authors contributed equally to this work.

References

Chang, SC, Jones, JD, Ellefson, RD and Ryan, RJ (1976). The porcine ovarian follicle: I. Selected chemical analysis of follicular fluid at different developmental stages. Biol Reprod 15, 321–8.CrossRefGoogle ScholarPubMed
Choi, K, Shim, J, Ko, N, Eom, H, Kim, J, Lee, JW, Jin, DI and Kim, H (2017). Production of heterozygous alpha-1,3-galactosyltransferase (GGTA1) knock-out transgenic miniature pigs expressing human CD39. Transgenic Res 26, 209–24.CrossRefGoogle ScholarPubMed
Collins, JL and Baltz, JM (1999). Estimates of mouse oviductal fluid tonicity based on osmotic responses of embryos. Biol Reprod 60, 1188–93.CrossRefGoogle ScholarPubMed
Downs, SM, Humpherson, PG and Leese, HJ (1998). Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol Reprod 58, 1084–94.CrossRefGoogle ScholarPubMed
Downs, SM, Humpherson, PG, Martin, KL and Leese, HJ (1996). Glucose utilization during gonadotropin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes. Mol Reprod Dev 44, 121–31.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Downs, SM and Utecht, AM (1999). Metabolism of radiolabeled glucose by mouse oocytes and oocyte-cumulus cell complexes. Biol Reprod 60, 1446–52.CrossRefGoogle ScholarPubMed
Erickson, GF and Shimasaki, S (2001). The physiology of folliculogenesis: the role of novel growth factors. Fertil Steril 76, 943–9.CrossRefGoogle ScholarPubMed
Funahashi, H, Cantley, TC, Stumpf, TT, Terlouw, SL and Day, BN (1994). Use of low-salt culture medium for in vitro maturation of porcine oocytes is associated with elevated oocyte glutathione levels and enhanced male pronuclear formation after in vitro fertilization. Biol Reprod 51, 633–9.CrossRefGoogle ScholarPubMed
Funahashi, H, Koike, T and Sakai, R (2008). Effect of glucose and pyruvate on nuclear and cytoplasmic maturation of porcine oocytes in a chemically defined medium. Theriogenology 70, 1041–7.CrossRefGoogle Scholar
Gilchrist, RB and Thompson, JG (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro . Theriogenology 67, 6–15.CrossRefGoogle ScholarPubMed
Ha, AN, Fakruzzaman, M, Lee, KL, Bang, JI, Deb, GK, Wang, Z and Kong, IK (2015). Effects of co-culture of cumulus oocyte complexes with denuded oocytes during in vitro maturation on the developmental competence of cloned bovine embryos. Reprod Domest Anim 50, 292–8.CrossRefGoogle ScholarPubMed
Hashimoto, S, Minami, N, Yamada, M and Imai, H (2000). Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol Reprod Dev 56, 520–6.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Hong, J and Lee, E (2007). Intrafollicular amino acid concentration and the effect of amino acids in a defined maturation medium on porcine oocyte maturation, fertilization, and preimplantation development. Theriogenology 68, 728–35.CrossRefGoogle Scholar
Kitagawa, T and Niimura, S (2006). Relationship between the size of perivitelline space and the incidence of polyspermy in porcine oocytes. Bull Facul Agric Niigata Univ 59, 21–6.Google Scholar
Kohata, C, Izquierdo-Rico, MJ, Romar, R and Funahashi, H (2013). Development competence and relative transcript abundance of oocytes derived from small and medium follicles of prepubertal gilts. Theriogenology 80, 970–8.CrossRefGoogle ScholarPubMed
Koo, DB, Kim, YJ, Yu, I, Kim, HN, Lee, KK and Han, YM (2005). Effects of in vitro fertilization conditions on preimplantation development and quality of pig embryos. Anim Reprod Sci 90, 101–10.CrossRefGoogle ScholarPubMed
Krisher, RL and Bavister, BD (1999). Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence. Mol Reprod Dev 53, 19–26.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Kwak, SS, Cheong, SA, Jeon, Y, Lee, E, Choi, KC, Jeung, EB and Hyun, SH (2012). The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 78, 86–101.CrossRefGoogle ScholarPubMed
Lawitts, JA and Biggers, JD (1992). Joint effects of sodium chloride, glutamine, and glucose in mouse preimplantation embryo culture media. Mol Reprod Dev 31, 189–94.CrossRefGoogle ScholarPubMed
Lee, J, You, J, Lee, GS, Hyun, SH and Lee, E (2013). Pig oocytes with a large perivitelline space matured in vitro show greater developmental competence after parthenogenesis and somatic cell nuclear transfer. Mol Reprod Dev 80, 753–62.CrossRefGoogle ScholarPubMed
Lee, J, Park, JI, Yun, JI, Lee, Y, Yong, H, Lee, ST, Park, CK, Hyun, SH, Lee, GS and Lee, E (2015). Rapamycin treatment during in vitro maturation of oocytes improves embryonic development after parthenogenesis and somatic cell nuclear transfer in pigs. J Vet Sci 16, 373–80.CrossRefGoogle ScholarPubMed
Lee, Y, Lee, H, Park, B, Elahi, F, Lee, J, Lee, ST, Park, CK, Hyun, SH and Lee, E (2016). Alpha-linolenic acid treatment during oocyte maturation enhances embryonic development by influencing mitogen-activated protein kinase activity and intraoocyte glutathione content in pigs. J Anim Sci 94, 3255–63.CrossRefGoogle ScholarPubMed
Lee, J, Lee, H, Lee, Y, Park, B, Elahi, F, Lee, ST, Park, CK, Hyun, SH and Lee, E (2017). In vitro oocyte maturation in a medium containing reduced sodium chloride improves the developmental competence of pig oocytes after parthenogenesis and somatic cell nuclear transfer. Reprod Fertil Dev 29, 1625–34.CrossRefGoogle Scholar
Li, J and Foote, RH (1996). Differential sensitivity of one-cell and two-cell rabbit embryos to sodium chloride and total osmolarity during culture into blastocysts. J Reprod Fertil 108, 307–12.CrossRefGoogle ScholarPubMed
Lin, ZL, Li, YH, Xu, YN, Wang, QL, Namgoong, S, Cui, XS and Kim, NH (2014). Effects of growth differentiation factor 9 and bone morphogenetic protein 15 on the in vitro maturation of porcine oocytes. Reprod Domest Anim 49, 219–27.CrossRefGoogle ScholarPubMed
Liu, RH, Li, YH, Jiao, LH, Wang, XN, Wang, H and Wang, WH (2002). Extracellular and intracellular factors affecting nuclear and cytoplasmic maturation of porcine oocytes collected from different sizes of follicles. Zygote 10, 253–60.CrossRefGoogle ScholarPubMed
O’Brien, JK, Dwarte, D, Ryan, JP, Maxwell, WM and Evans, G (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod Fertil Dev 8, 1029–37.CrossRefGoogle ScholarPubMed
Sato, H, Iwata, H, Hayashi, T, Kimura, K, Kuwayama, T and Monji, Y (2007). The effect of glucose on the progression of the nuclear maturation of pig oocytes. Anim Reprod Sci 99, 299–305.CrossRefGoogle ScholarPubMed
Son, YJ, Lee, SE, Park, YG, Jeong, SG, Shin, MY, Kim, EY and Park, SP (2018). Fibroblast growth factor 10 enhances the developmental efficiency of somatic cell nuclear transfer embryos by accelerating the kinetics of cleavage during in vitro maturation. Cell Reprogram 20, 196–204.CrossRefGoogle ScholarPubMed
Song, BS, Jeong, PS, Lee, JH, Lee, MH, Yang, HJ, Choi, SA, Lee, HY, Yoon, SB, Park, YH, Jeong, KJ, Kim, YH, Jin, YB, Kim, JS, Sim, BW, Huh, JW, Lee, SR, Koo, DB, Chang, KT and Kim, SU (2018). The effects of kinase modulation on in vitro maturation according to different cumulus–oocyte complex morphologies. PLoS One 13, e0205495.CrossRefGoogle ScholarPubMed
Steeves, TE and Gardner, DK (1999). Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows. Mol Reprod Dev 54, 92–101.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
Sun, MH, Zheng, J, Xie, FY, Shen, W, Yin, S and Ma, JY (2015). Cumulus cells block oocyte meiotic resumption via gap junctions in cumulus oocyte complexes subjected to DNA double-strand breaks. PLoS One 10, e0143223.CrossRefGoogle ScholarPubMed
Taweechaipaisankul, A, Jin, JX, Lee, S, Kim, GA and Lee, BC (2016). The effects of canthaxanthin on porcine oocyte maturation and embryo development in vitro after parthenogenetic activation and somatic cell nuclear transfer. Reprod Domest Anim 51, 870–6.CrossRefGoogle ScholarPubMed
Yamauchi, N, Sasada, H, Soloy, E, Dominko, T, Kikuchi, K and Nagai, T (1999). Effects of hormones and osmolarity in the culture medium on germinal vesicle breakdown of porcine oocytes. Theriogenology 52, 153–62.CrossRefGoogle ScholarPubMed
Yoshioka, K, Suzuki, C, Tanaka, A, Anas, IM and Iwamura, S (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol Reprod 66, 112–9.CrossRefGoogle Scholar
You, J, Lee, J, Hyun, SH and Lee, E (2012). l-Carnitine treatment during oocyte maturation improves in vitro development of cloned pig embryos by influencing intracellular glutathione synthesis and embryonic gene expression. Theriogenology 78, 235–43.CrossRefGoogle ScholarPubMed
Vanderhyden, BC, Caron, PJ, Buccione, R and Eppig, JJ (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol 140, 307–17.CrossRefGoogle ScholarPubMed
Wang, WH, Abeydeera, LR, Cantley, TC and Day, BN (1997). Effects of oocyte maturation media on development of pig embryos produced by in vitro fertilization. J Reprod Fertil 111, 101–8.CrossRefGoogle ScholarPubMed
Wen, J, Wang, GL, Yuan, HJ, Zhang, J, Xie, HL, Gong, S, Han, X and Tan, JH (2020). Effects of glucose metabolism pathways on nuclear and cytoplasmic maturation of pig oocytes. Sci Rep 10, 2782. CrossRefGoogle ScholarPubMed
Xie, HL, Wang, YB, Jiao, GZ, Kong, DL, Li, Q, Li, H, Zheng, LL and Tan, JH (2016). Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Sci Rep 6, 20764. CrossRefGoogle ScholarPubMed
Zhang, L, Jiang, S, Wozniak, PJ, Yang, X and Godke, RA (1995). Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro . Mol Reprod Dev 40, 338–44.CrossRefGoogle ScholarPubMed